Consolidation of Fear Extinction Requires NMDA Receptor-Dependent Bursting in the Ventromedial Prefrontal Cortex

Neuron

Volumn 53, Issue 6, 2007, Pages 871-880

  Burgos Robles, Anthony ^a   Vidal Gonzalez, Ivan ^a   Santini, Edwin ^a   Quirk, Gregory J ^a  

^a PONCE SCHOOL OF MEDICINE   (Puerto Rico)

Author keywords

HUMDISEASE; PROTEINS; SYSNEURO

Indexed keywords

N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR BLOCKING AGENT;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FEAR; MALE; NONHUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; RAT; RECALL; REINFORCEMENT; TRAINING;

ACTION POTENTIALS; ANALYSIS OF VARIANCE; ANIMALS; BEHAVIOR, ANIMAL; CONDITIONING (PSYCHOLOGY); DOSE-RESPONSE RELATIONSHIP, DRUG; EXCITATORY AMINO ACID ANTAGONISTS; EXTINCTION, PSYCHOLOGICAL; FEAR; MALE; NEURONS; PIPERAZINES; PREFRONTAL CORTEX; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, N-METHYL-D-ASPARTATE; TIME FACTORS;

EID: 33847662076     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuron.2007.02.021     Document Type: Article

References (61)

1. Abraham W.C., and Mason S.E. Effects of the NMDA receptor/channel antagonists CPP and MK801 on hippocampal field potentials and long-term potentiation in anesthetized rats. Brain Res. 462 (1988) 40-46
2. Baker J.D., and Azorlosa J.L. The NMDA antagonist MK-801 blocks the extinction of Pavlovian fear conditioning. Behav. Neurosci. 110 (1996) 618-620
3. Barrett D., Shumake J., Jones D., and Gonzalez-Lima F. Metabolic mapping of mouse brain activity after extinction of a conditioned emotional response. J. Neurosci. 23 (2003) 5740-5749
4. Berlau D.J., and McGaugh J.L. Enhancement of extinction memory consolidation: the role of the noradrenergic and GABAergic systems within the basolateral amygdala. Neurobiol. Learn. Mem. 86 (2006) 123-132
5. Blair H.T., Schafe G.E., Bauer E.P., Rodrigues S.M., and LeDoux J.E. Synaptic plasticity in the lateral amygdala: a cellular hypothesis of fear conditioning. Learn. Mem. 8 (2001) 229-242
6. Blanchard D.C., and Blanchard R.J. Innate and conditioned reactions to threat in rats with amygdaloid lesions. J. Comp. Physiol. Psychol. 81 (1972) 281-290
7. Bliss T.V., and Collingridge G.L. A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361 (1993) 31-39
8. Bouton M.E., Westbrook R.F., Corcoran K.A., and Maren S. Contextual and temporal modulation of extinction: behavioral and biological mechanisms. Biol. Psychiatry 60 (2006) 352-360
9. Buzsaki G., Csicsvari J., Dragoi G., Harris K., Henze D., and Hirase H. Homeostatic maintenance of neuronal excitability by burst discharges in vivo. Cereb. Cortex 12 (2002) 893-899
10. Corcoran K.A., and Quirk G.J. Activity in prelimbic cortex is necessary for the expression of learned, but not innate, fears. J. Neurosci. 27 (2007) 840-844
11. Corcoran K.A., Desmond T.J., Frey K.A., and Maren S. Hippocampal inactivation disrupts the acquisition and contextual encoding of fear extinction. J. Neurosci. 25 (2005) 8978-8987
12. Davis M. Role of NMDA receptors and MAP kinase in the amygdala in extinction of fear: clinical implications for exposure therapy. Eur. J. Neurosci. 16 (2002) 395-398
13. Davis M., and Whalen P.J. The amygdala: vigilance and emotion. Mol. Psychiatry 6 (2001) 13-34
14. Davis M., Myers K.M., Chhatwal J., and Ressler K.J. Pharmacological treatments that facilitate extinction of fear: relevance to psychotherapy. NeuroRx 3 (2006) 82-96
15. Elgersma Y., and Silva A.J. Molecular mechanisms of synaptic plasticity and memory. Curr. Opin. Neurobiol. 9 (1999) 209-213
16. Falls W.A., Miserendino M.J., and Davis M. Extinction of fear-potentiated startle: blockade by infusion of an NMDA antagonist into the amygdala. J. Neurosci. 12 (1992) 854-863
17. Foa E.B. Psychosocial treatment of posttraumatic stress disorder. J. Clin. Psychiatry 61 Suppl 5 (2000) 43-48
18. Gold J.I., and Bear M.F. A model of dendritic spine Ca2+ concentration exploring possible bases for a sliding synaptic modification threshold. Proc. Natl. Acad. Sci. USA 91 (1994) 3941-3945
19. Gureviciene I., Puolivali J., Pussinen R., Wang J., Tanila H., and Ylinen A. Estrogen treatment alleviates NMDA-antagonist induced hippocampal LTP blockade and cognitive deficits in ovariectomized mice. Neurobiol. Learn. Mem. 79 (2003) 72-80
20. Harris K.D., Hirase H., Leinekugel X., Henze D.A., and Buzsaki G. Temporal interaction between single spikes and complex spike bursts in hippocampal pyramidal cells. Neuron 32 (2001) 141-149
21. Herry C., and Garcia R. Prefrontal cortex long-term potentiation, but not long-term depression, is associated with the maintenance of extinction of learned fear in mice. J. Neurosci. 22 (2002) 577-583
22. Herry C., Trifilieff P., Micheau J., Luthi A., and Mons N. Extinction of auditory fear conditioning requires MAPK/ERK activation in the basolateral amygdala. Eur. J. Neurosci. 24 (2006) 261-269
23. Hofmann S.G., Meuret A.E., Smits J.A., Simon N.M., Pollack M.H., Eisenmenger K., Shiekh M., and Otto M.W. Augmentation of exposure therapy with D-cycloserine for social anxiety disorder. Arch. Gen. Psychiatry 63 (2006) 298-304
24. Hugues S., Deschaux O., and Garcia R. Postextinction infusion of a mitogen-activated protein kinase inhibitor into the medial prefrontal cortex impairs memory of the extinction of conditioned fear. Learn. Mem. 11 (2004) 540-543
25. Hugues S., Chessel A., Lena I., Marsault R., and Garcia R. Prefrontal infusion of PD098059 immediately after fear extinction training blocks extinction-associated prefrontal synaptic plasticity and decreases prefrontal ERK2 phosphorylation. Synapse 60 (2006) 280-287
26. Ishikawa A., and Nakamura S. Convergence and interaction of hippocampal and amygdalar projections within the prefrontal cortex in the rat. J. Neurosci. 23 (2003) 9987-9995
27. Jackson M.E., Homayoun H., and Moghaddam B. NMDA receptor hypofunction produces concomitant firing rate potentiation and burst activity reduction in the prefrontal cortex. Proc. Natl. Acad. Sci. USA 101 (2004) 8467-8472
28. Kalisch R., Korenfeld E., Stephan K.E., Weiskopf N., Seymour B., and Dolan R.J. Context-dependent human extinction memory is mediated by a ventromedial prefrontal and hippocampal network. J. Neurosci. 26 (2006) 9503-9511
29. Lamprecht R., and LeDoux J. Structural plasticity and memory. Nat. Rev. Neurosci. 5 (2004) 45-54
30. Lebron K., Milad M.R., and Quirk G.J. Delayed recall of fear extinction in rats with lesions of ventral medial prefrontal cortex. Learn. Mem. 11 (2004) 544-548
31. LeDoux J.E. Emotion circuits in the brain. Annu. Rev. Neurosci. 23 (2000) 155-184
32. Lin C.H., Yeh S.H., Lu H.Y., and Gean P.W. The similarities and diversities of signal pathways leading to consolidation of conditioning and consolidation of extinction of fear memory. J. Neurosci. 23 (2003) 8310-8317
33. Magee J.C., and Johnston D. A synaptically controlled, associative signal for Hebbian plasticity in hippocampal neurons. Science 275 (1997) 209-213
34. Maren S., and Quirk G.J. Neuronal signalling of fear memory. Nat. Rev. Neurosci. 5 (2004) 844-852
35. Milad M.R., and Quirk G.J. Neurons in medial prefrontal cortex signal memory for fear extinction. Nature 420 (2002) 70-74
36. Milad M.R., Wright C.I., Orr S.P., Pitman R.K., Quirk G.J., and Rauch S.L. Recall of fear extinction in humans activates the ventromedial prefrontal cortex and hippocampus in concert. Biol. Psychiatry (2006) in press
37. Morgan M.A., Romanski L.M., and LeDoux J.E. Extinction of emotional learning: contribution of medial prefrontal cortex. Neurosci. Lett. 163 (1993) 109-113
38. Myers K.M., and Davis M. Mechanisms of fear extinction. Mol. Psychiatry 12 (2007) 120-150
39. O'Neill K.A., and Liebman J.M. Unique behavioral effects of the NMDA antagonist, CPP, upon injection into the medial pre-frontal cortex of rats. Brain Res. 435 (1987) 371-376
40. Paré D., Quirk G.J., and LeDoux J.E. New vistas on amygdala networks in conditioned fear. J. Neurophysiol. 92 (2004) 1-9
41. Paulsen O., and Sejnowski T.J. Natural patterns of activity and long-term synaptic plasticity. Curr. Opin. Neurobiol. 10 (2000) 172-179
42. Paxinos G., and Watson C. The Rat Brain in Stereotaxic Coordinates (1998), Academic Press, San Diego
43. Phelps E.A., Delgado M.R., Nearing K.I., and LeDoux J.E. Extinction learning in humans: role of the amygdala and vmPFC. Neuron 43 (2004) 897-905
44. Pike F.G., Meredith R.M., Olding A.W., and Paulsen O. Rapid report: postsynaptic bursting is essential for 'Hebbian' induction of associative long-term potentiation at excitatory synapses in rat hippocampus. J. Physiol. 518 (1999) 571-576
45. Quirk G.J. Memory for extinction of conditioned fear is long-lasting and persists following spontaneous recovery. Learn. Mem. 9 (2002) 402-407
46. Quirk G.J., Russo G.K., Barron J.L., and Lebron K. The role of ventromedial prefrontal cortex in the recovery of extinguished fear. J. Neurosci. 20 (2000) 6225-6231
47. Ressler K.J., Rothbaum B.O., Tannenbaum L., Anderson P., Graap K., Zimand E., Hodges L., and Davis M. Cognitive enhancers as adjuncts to psychotherapy: use of D-cycloserine in phobic individuals to facilitate extinction of fear. Arch. Gen. Psychiatry 61 (2004) 1136-1144
48. Richardson R., Ledgerwood L., and Cranney J. Facilitation of fear extinction by D-cycloserine: theoretical and clinical implications. Learn. Mem. 11 (2004) 510-516
49. Riedel G., Platt B., and Micheau J. Glutamate receptor function in learning and memory. Behav. Brain Res. 140 (2003) 1-47
50. Rothbaum B.O., and Davis M. Applying learning principles to the treatment of post-trauma reactions. Ann. N Y Acad. Sci. 1008 (2003) 112-121
51. Santini E., Muller R.U., and Quirk G.J. Consolidation of extinction learning involves transfer from NMDA-independent to NMDA-dependent memory. J. Neurosci. 21 (2001) 9009-9017
52. Santini E., Ge H., Ren K., Pena D.O., and Quirk G.J. Consolidation of fear extinction requires protein synthesis in the medial prefrontal cortex. J. Neurosci. 24 (2004) 5704-5710
53. Shi W.X., and Zhang X.X. Dendritic glutamate-induced bursting in the prefrontal cortex: further characterization and effects of phencyclidine. J. Pharmacol. Exp. Ther. 305 (2003) 680-687
54. Sierra-Mercado Jr. D., Corcoran K.A., Lebron-Milad K., and Quirk G.J. Inactivation of the ventromedial prefrontal cortex reduces expression of conditioned fear and impairs subsequent recall of extinction. Eur. J. Neurosci. 24 (2006) 1751-1758
55. Sotres-Bayon F., Cain C.K., and LeDoux J.E. Brain mechanisms of fear extinction: historical perspectives on the contribution of prefrontal cortex. Biol. Psychiatry 60 (2006) 329-336
56. Sotres-Bayon F., Bush D.E., and LeDoux J.E. Acquisition of fear extinction requires activation of NR2B-containing NMDA receptors in the lateral amygdala. Neuropsychopharmacology (2007) 10.1038/sj.npp.1301316 in press. Published online January 10, 2007
57. Suzuki A., Josselyn S.A., Frankland P.W., Masushige S., Silva A.J., and Kida S. Memory reconsolidation and extinction have distinct temporal and biochemical signatures. J. Neurosci. 24 (2004) 4787-4795
58. Tierney P.L., Degenetais E., Thierry A.M., Glowinski J., and Gioanni Y. Influence of the hippocampus on interneurons of the rat prefrontal cortex. Eur. J. Neurosci. 20 (2004) 514-524
59. Walker D.L., and Davis M. The role of amygdala glutamate receptors in fear learning, fear-potentiated startle, and extinction. Pharmacol. Biochem. Behav. 71 (2002) 379-392
60. Wayner M.J., Tracy H.A., Armstrong D.L., and Phelix C.F. Air righting: role of the NMDA receptor channel and hippocampal LTP. Physiol. Behav. 69 (2000) 505-510
61. Zhang X.X., and Shi W.X. Dendritic glutamate-induced bursting in prefrontal pyramidal cells: role of NMDA and non-NMDA receptors. Acta Pharmacologica Sinica 20 (1999) 1125-1131